Skeletal muscle regeneration relies on the orchestrated interaction of myogenic and non-myogenic cells with spatial and temporal coordination. The regenerative capacity of skeletal muscle declines with aging due to alterations in myogenic stem/progenitor cell states and functions, non-myogenic cell contributions, and systemic changes, all of which accrue with age. A holistic network-level view of the cell-intrinsic and -extrinsic changes influencing muscle stem/progenitor cell contributions to muscle regeneration across lifespan remains poorly resolved. To provide a comprehensive atlas of regenerative muscle cell states across mouse lifespan, we collected a compendium of >270,000 single-cell transcriptomes from hindlimb muscles of young, old, and geriatric (4-26 months-old) mice at six closely sampled time-points following myotoxin injury. We identified 29 muscle-resident cell types, eight of which exhibited accelerated or delayed dynamics in their abundances between age groups, including T and NK cells and multiple monocyte/macrophage subtypes, suggesting that the age-related decline in muscle repair may arise from temporal miscoordination of the inflammatory response. We performed a pseudotime analysis of myogenic cells across the regeneration timespan and found age-specific myogenic stem/progenitor cell trajectories in old and geriatric muscles. Given the critical role that cellular senescence plays in limiting cell contributions in aged tissues, we built a series of tools to bioinformatically identify senescence in these single-cell data and assess their ability to identify senescence within key myogenic stages. By comparing single-cell senescence scores to co-expression of hallmark senescence genes Cdkn2a and Cdkn1a, we found that a gene list experimentally derived from a muscle foreign body response (FBR) fibrosis model accurately identified senescent-like myogenic cells across mouse ages, injury time-points, and cell-cycle states, in a manner comparable to curated gene lists. Further, this scoring approach in both single-cell and spatial transcriptomic datasets pinpointed transitory senescent-like subsets within the myogenic stem/progenitor cell trajectory that are associated with stalled MuSC self-renewal states across all ages of mice. This new resource of mouse skeletal muscle aging provides a comprehensive portrait of the changing cellular states and interactions underlying skeletal muscle regeneration across mouse lifespan.